Evolutionary papers: he role of
psychological factors in questionnaire-based studies on routes of human
toxoplasmosis transmission: The raw meat consumption but not the contact with
cats is the major risk factor.

This paper studies impacts of particular toxoplasmosis-risk factors
(consumption of raw meat and contact with cats), their interactions, and their
relationship with the personality of the subjects. Among 243 men and 343 women
the frequency of subjects with antitoxoplasma immunity was 26.6 percent and
21.6 %, respectively. The association of antitoxoplasma immunity with the two
risk factors was estimated by log-linear analysis. Reported contact with cats
has no influence on the probability of having antitoxoplasma immunity (p=0.23)
while the consumption of raw meat increased this probability (p=0.0008). Very
strong positive association between the contact with cats and the raw meat
consumption was found among subjects without toxoplasmosis (p=0.0028),
suggesting that among these persons some subjects either incorrectly assessed
their exposition to the risk factors or provided false data during the
interview. The results of logistic regression suggest that the contact with cat
and the consumption of raw meat are associated with particular personality
traits. However, these traits differ from those associated with antitoxoplasma
immunity suggesting that the correlation between antitoxoplasma immunity and
consumption of raw meat reflects epidemiological importance of the raw meat
rather than a correlation of both factors (raw meat consumption and probability
of acquiring toxoplasmosis) with the subjects personality.

e probability of having antitoxoplasma immunity (p=0.23)
while the consumption of raw meat increased this probability (p=0.0008).
Very strong positive association between the contact with cats and the raw meat
consumption was found among subjects without toxoplasmosis (p=0.0028),
suggesting that among these persons some subjects either incorrectly assessed
their exposition to the risk factors or provided false data during the
interview. The results of logistic regression suggest that the contact with cat
and the consumption of raw meat are associated with particular personality
traits. However, these traits differ from those associated with antitoxoplasma
immunity suggesting that the correlation between antitoxoplasma immunity and
consumption of raw meat reflects epidemiological importance of the raw meat
rather than a correlation of both factors (raw meat consumption and probability
of acquiring toxoplasmosis) with the subjects personality.

Toxoplasmosis is an
infectious disease caused by the parasite Toxoplasmagondii.
It is one of the most common protozoan diseases in animals and man. The
prevalence of serum antibodies to Toxoplasma varies from less than 5
percent in Navajo Indians, Australian aborigines, and Eskimos (1) to more than
80 percent in Parisians (2). T. gondii is an economically important
cause of disease in animals and produces a variety of clinical manifestation in
humans (3,4).

Except intrauterine
transmission, there are two main natural routes of infection with Toxoplasma:
the faecal-oral, i.e., infection by the oocyst from contact with infected
definitive hosts, the cat or exposure to contaminated soil, and the
carnivorism, i.e., infection by tissue cysts through ingestion of raw or
undercooked meat of intermediate hosts. The relative importance in human
population of these two routes varies from one report to another, depending on
hygienic, sociological and geographical factors in the survey area and on
occupations, socioeconomical status and customs of the inhabitants (5).

Despite the long tradition of
toxoplasmosis studies, there is still a controversy concerning the main route
of T. gondii infection in many countries, including the Czech Republic
(6). The epidemiological importance of the two potential risk factors, the
contact with cats and the consumption of raw or undercooked meat, is mostly
studied in an indirect way, either by questionnaire survey or by interview with
infected subjects. Evidently, many subjective factors and biases might obscure
the results of such studies. Recently, the difference in personality profiles
between Toxoplasma-infected and Toxoplasma-free subjects was
reported (7,8). The probability of the consumption of raw meat and the contact
with cats probably also depends on the subject personality. Therefore, we
suspect that the association between toxoplasmosis and reported exposition to
some "risk factor" could simply reflect a correlation of both T.
gondii infection and the studied "risk factor" with the same
factor, namely with the subject personality.

In this study the prevalence
of antitoxoplasma immunity and associated epidemiological factors were
investigated on the group of 586 biology students and biologists. In contrast
to previous studies we focused our attention not only on the study of
particular risk factors but also on their interactions and their relationship
with the personality (and behavior) of the subjects.

METHODS

Subjects

The data were collected over
a period of 40 months in 1992-1995. The experimental group was composed of 243
men and 343 women, mostly biology students and biologists of the Faculty of
Science, Charles University, Prague. For stratified analyses the subjects were
sorted into three age categories, 18-24 (n=396), 25-31 (n=97),
and 32-65 (n=93). The subjects were interviewed by authors about
toxoplasmosis risk factors. They were asked: 1. Do (did) you often play with
cats or kitten and/or have (or had) you a cat in your household? 2. Do (or did)
you ever eat raw meat or food containing raw meat and/or do (or did) you ever
taste raw meat or a raw meat paste when cooking? Three hundred and eighty-four
(384) subjects gave either positive or negative answer on at least one
question. Most of the subjects also completed Cattell's personality
questionnaire (243 men and 200 women). After the interview and completing the
questionnaire the subjects were tested for antitoxoplasma immunity. All
subjects gave their informed consent before they were accepted for the study.

Immunological test
for antitoxoplasma immunity

The antitoxoplasma cellular
immunity of experimental subjects was assessed by an intradermal delayed
hypersensitivity test (IDHT) (9). This test yields presence/absence data. The
assay was performed using Toxoplasmin as antigen and sham injection of control
antigen (both produced by SEVAC, USOL Prague) as negative control. Positive
reactions were of the delayed tuberculin type and were assessed 48 hours after
antigen administration. The large-scale use of the skin test in population
surveys has shown excellent correlation between the results of this test and
the latent T. gondii infection (10). Development of the ability to
elicit delayed hypersensitivity to Toxoplasma antigens in man requires
a period of months or even years after initial infection. Therefore, it is
practically useless for diagnosis of acute toxoplasmosis. However, the
hypersensitivity usually persists for the life of the host so it is the most
useful method in the diagnosis of latent infections (10).

Personality tests

Cattell's sixteen factor
questionnaire (form A) (11) was used for the characterization of personality.
This questionnaire is widely used for personality studies in many countries,
including Czech Republic (12,13). It covers sixteen personality factors
(Sizothymia/Affectothymia, Intelligence, Strength of ego,
Submissiveness/Dominance, Desurgency/Surgency, Superego strength,
Threctia/Parmia, Harria/Premsia, Alaxia/Protension, Praxernia/Autia,
Naivete/Shrewdness, Guilt proneness, Conservatism/Radicalism, Group dependency,
Self sentiment integration, Ergic tension). For each factor the test provides a
value on 27-points row scale (which can be transformed for age/sex standardized
value on 10-points standardized scale). The main advantage of this traditional
personality test is that it contains only one hundred and eighty-seven (187)
questions. Therefore, most subjects can complete it within one hour. All
subjects (except twenty-two parasitologists) completed their questionnaires before
the results of the toxoplasmosis test were known.

Statistical Methods

The effects of the risk
factors (raw meat consumption and cat contact), confounding variables (gender,
age) and their interactions were estimated by log-linear analysis. The
correlation between the risk factors and the personality profile was quantified
by logistic regression using either cat or raw meat as a dichotomous dependent
variable and the raw personality factors and confounding variables (gender and
age) as in depended variables. The raw personality factors instead of
age-standardized ones were used in statistical analysis to prevent information
loss during the transformation of twenty seven-point raw scales into ten-point
age-standardized scales and to avoid an application of general population-based
correction factors on the highly "nonstandard" subpopulation of
biologists. The EpiInfo 6.01 program was used for a stratified log linear
analysis and Statistica® program for all other statistical testing.

Two hundred and forty-three
(243) men and three hundred and forty-three (343) women were tested for
cellular immunity against T. gondii. Among the men and the women
frequency of subjects with antitoxoplasma immunity was 26.6 percent and 21.6
percent, respectively. Before the results of immunological tests were known,
the subjects completed the Cattell´s 16 personality factors questionnaire and
answered two questions concerning two potential Toxoplasma-infection risk
factors. All men (243) and two hundred (200) women completed the questionnaire
and three hundred and eighty-four (384) subjects gave either positive or negative
answer on at least one risk factor-question. According to their answers the
subjects were sorted into four groups: cat minus meat minus, cat plus meat
minus, cat minus meat plus, and cat plus meat plus. The frequencies of
toxoplasma positive (TP) and toxoplasma negative (TN) subjects (the subjects
with and without antitoxoplasma immunity) in each group were calculated (Tab.
1a-c). The association of antitoxoplasma immunity with raw meat consumption and
cat contact was estimated by log-linear analysis. The results of simple
analysis of 2 x 2 contingency tables showed that the reported contact with cats
has either none or only marginal influence on the probability of being
toxoplasma positive. Among 215 subjects reporting the contact with a cat, the
frequency of toxoplasmosis was 27.0 percent while among 161 subjects without
the contact the frequency of antitoxoplasma immunity was 23.6 percent. The
difference between the two sets was not statistically significant (p=0.23,
n=376, one tailed test). On the other hand, the consumption of raw
meat significantly increased the probability of being toxoplasmosis positive.
Among 172 subjects who reported the consumption of raw meat the frequency of
antitoxoplasma immunity was 32.0 percent while among the remaining 196 subjects
the frequency was only 17.9 percent (p=0.0008, n=368, one
tailed test). The association between the consumption of raw meat and the
antitoxoplasma immunity was significant both for men (33.8 percent versus 14.6
percent, p= 0.010, n=113, one tailed test) and women (30.8
percent versus 18.9 percent, p=0.014, n=255, one tailed
test).

To reveal possible
interactions between the risk factors, the best model for explaining our data
was searched for by log-linear analysis. The model included following dichotomous
factors: gender (1), antitoxoplasma immunity (2), cat (3) and raw meat (4). The
best model obtained by standard automatic procedure was 1-4, 2-4, 3-4 (Chi
square=3.33, df=8, p=0.91). Despite the existence of the difference in
prevalence of antitoxoplasma immunity among men and women, the inclusion of the
1-2 interaction (gender specific differences in toxoplasmosis susceptibility)
had no effect on the model explanatory power (Chi square=3.34, df=7, p=0.85).
It suggests that the difference in prevalence can be explained by interaction
1-4, i.e., by gender specific difference in the consumption of raw meat. Also
the inclusion of interaction 2-3 (association of the contact with cats with
antitoxoplasma immunity) did not improve the model (Chi square=3.32, df=7, p=0.85).
On the other hand the interaction 3-4 (association between the contact with
cats and the raw meat consumption) was very important. The model 1-4, 2-4, 3
(Chi square=11.21, df=9, p=0.26) was significantly worse (Chi
square=7.88, df=1, p=0.005) than the model 1-4, 2-4, 3-4. The
interaction between the contact with cats and the raw meat consumption can
probably explain (in combination with the interaction 2-4, e.g., the
correlation of antitoxoplasma immunity with the raw meat compsumption) the
higher prevalence of subjects with antitoxoplasma immunity among those with the
reported contact with cat. Very strong positive association between these two
risk factors was found in the TN subset (Tab 1c). The frequencies of subjects
reporting the contact with a cat were 66.4 percent and 48.1 percent among 113
raw meat plus and among 158 raw meat minus subjects, respectively (p=0.0028,
n=271, two tailed test). No association between the cat and the raw meat
was observed in TP subset 61.1 percent versus 57.1 percent (p=0.71, n=89,
two tailed test) (see Tab. 1c).

TABLE 1. Frequency tables
for antitoxoplasma immunity and two risk factors. Tabs. 1a and 1b show the
association of antitoxoplasma immunity with raw meat consumption and contacts
with cats, respectively. Tab 1c shows the association of two T.
gondii-infection risk factors. The absolute numbers of the subjects in each
subset are given.

1a

(men/women)

raw meat
minus

raw meat
plus

toxoplasma
negative

41/120

43/74

toxoplasma
positive

7/28

22/33

1b

(men/women)

cat
minus

cat plus

toxoplasma
negative

35/88

51/106

toxoplasma
positive

13/25

21/37

1 c

(toxo
negative/positive)

raw
meat minus

raw meat
plus

cat minus

82/15

38/21

cat plus

76/20

75/33

Influence of
confoundings, gender and age, on meat-antitoxoplasma immunity interaction.

For the estimation of
importance of the effects of the main risk factor, the raw meat, and
confounding variables (gender, age), we used the logistic regression with
either the antitoxoplasma immunity or raw meat consumption as the dependent
dichotomous variable. The results (including the estimations of odds ratios)
are shown in Tabs 2, 3. The effect of the confounding variables was studied
also by a stratified log-linear analysis. Mantel-Haenszel weighted odds ratio
for meat-antitoxoplasma immunity interaction was 2.16 (95 percent confidence interval
1.32-3.52). The result of the test does not suggest that odds ratios differ by
age-stratum (Chi square=0.51, p=0.774). The same conclusions were
obtained by the gender-stratified log-linear analysis (Chi square=0.62, p=
0.429).

Influence of human
personality on reporting a contact with cat or raw meat consumption.

The Toxoplasma
infection of human subjects is associated with a shift of certain personality
factors (Low superego strength and Protension for men, and Affectothymia for
women) (7, 8). The probability of reporting a contact with cat or raw meat
consumption can also be influenced by the subjects personality. Therefore, the
association between the raw meat consumption and the antitoxoplasma immunity
can simply reflect a correlation of both the reporting of raw meat consumption
and the T. gondii infection with the subject's personality. To exclude
this possibility we measured the personality profiles of 243 men (69 Toxoplasma
infected and 174 Toxoplasma free) and 200 women (44 Toxoplasma
infected and 156 Toxoplasma free) from our biology students set. The
correlation between the personality profiles and two risk factors (cat and raw
meat) was estimated by logistic regression using contact with cat or raw meat
consumption as the dependent dichotomous variable and 16 raw personality
factors and age as the continuous independent variables (Tabs 4, 5). It is
evident, that both the contact with cat and the consumption of raw meat are
associated with particular personality traits. However, these traits differ
from those associated with antitoxoplasma immunity.

TABLE 5 Correlation of
the reported consumption of raw meat with personality profile

Model: Logistic regression
(logit). Dep. var: MEAT (0-raw meat minus (n=98) or 1-raw meat plus (n=96)
subjects). Loss: Max likelihood (MS-err. scaled to 1). Final loss: 120.7
Chi(17)=27.54 p=0.051. The third line shows constant B0 and beta estimates of
the regression function. The first and second line shows arithmetic mean of raw
personality factors for subject with and without reported consumption of raw
meat, respectively. For the list of personality factors see the Tab 4.

Const.B0

A

B

C

E

F

G

H

I

L

M

N

O

Q1

Q2

Q3

Q4

AGE

Mean 0

9.78

9.41

13.3

12.2

11.7

9.10

9.18

12.7

9.52

13.1

8.20

10.7

7.33

13.2

10.1

13.3

25.39

Mean 1

10.4

9.29

13.0

13.7

12.7

9.88

11.7

12.5

10.4

13.3

8.06

10.4

7.64

12.8

10.3

14.5

30.29

Estimate

-1.6

-.02

-.02

-.06

-.01

.064

.007

.083

-.05

-.00

-.01

-.02

-.08

.003

.017

.035

.098

.035

Std.Err.

1.05

.055

.076

.057

.044

.051

.050

.043

.051

.061

.055

.059

.051

.062

.061

.060

.044

.016

t(176)

-1.5

-.37

-.33

-1.0

-.09

1.25

.138

1.96

-.91

-.02

-.35

-.38

-1.5

.054

.279

.574

2.22

2.180

p-level

.142

.715

.745

.297

.921

.214

.890

.052

.366

.986

.728

.708

.142

.957

.780

.566

.028

.031

DISCUSSION

Our results suggest that in
the Czech Republic the important risk factor for acquiring T. gondii
infection is eating or tasting raw meat. On the other hand the contact with cat
seems to play either none or only a minor role.

Raw meat containing T.
gondii tissue cysts is known to be an important source of infection
(14,15). Its importance varies from one area to another, depending on eating
habits. In comparison with similar studies from others countries, our results
showed a very tight association between the consumption of raw meat and the
antitoxoplasma immunity. This can be partially explained by the fact that our
question covered both the eating and the tasting of raw meat. Many housewives
have probably the habit of tasting raw meat such as a paste from chopped pork
for meat balls during cooking. They might forget to report this habit when
asked about the consumption of raw meat.

The absence of correlation
between raw meat and the T.gondii infection was reported in several
previous studies (16-19). These negative results, however, must be interpreted
with a caution. The prevalence of tissue cysts in meat of different animals
extremely varies. The highest prevalence is usually reported in sheep (9-23
percent) and pigs (12-15 percent), the lowest in cattle (0-10 percent) and hens
(0.3-8 percent) (20). Eating of hamburgers or other meals from raw or
undercooked beef probably represents only minor risk of inquiring toxoplasmosis.

Our results indicate that the
strength of the association between raw meat and toxoplasmosis might in fact be
even higher then suggested by basic statistical analysis of contingency tables.
The strong association between the contact with a cat and the raw meat
consumption that exists in the TN subset suggests that the results of
questionnaire studies might be obscured by subjects who intentionally or
unintentionally provided incorrect information during the interview. The
surplus of double-plus subjects (the ones that gave positive answer about cat
and raw meat) in the TN subset suggests that some subjects either a priori
believe to be at higher risk of infection or believe that the investigator will
be pleased by obtaining positive answers to his questions. Such subjects will
answer both questions positively. It is indicative that the association between
the cat and the raw meat does not exist in the TP subset. Most of the members
of this subset probably correctly reported the consumption of raw meat (otherwise
they would not enter TP subset). On the other hand, most subjects reporting
consumption of raw meat in the TN subset probably provided incorrect
information (otherwise they would enter TP subset) and many of them probably
also provided incorrect information reporting the contact with a cat. If we
could eliminate these subjects from TN subset the strength of the association
between consuming raw meat and the antitoxoplasma immunity would even increase.

According to our results,
contact with cats did not affect the probability of being toxoplasma infected.
It has already been pointed out by many authors that the role of cat in T.
gondii life cycle should not be confused with its role in direct
transmission of human toxoplasmosis (21). Absence of an association between the
contact with cat and the antitoxoplasma immunity is in a good agreement with
results of many but not all (17-19,22, 23) previous studies. Authors mostly
found no or low association between toxoplasmosis and the contact with cats (15,16,24-26).
Sometimes a modest increase of prevalence of toxoplasmosis was observed among
breeders of pedigree cats (24). This increase is usually interpreted as the
results of handling of raw offal (27). The increased prevalence among cat
owners can be also explained by the facts that the ownership of a cat may be
associated not only with the handling raw meat but also with the ownership of
other animals. Several studies showed a dramatic increase of toxoplasmosis
prevalence among rabbits owners (28,29). It can be also argued that if cats
were important vectors, one would expect to see an increased incidence of
disease among children and the elderly. Toxoplasmosis, however, is largely a
disease of young adult (30).

Our finding of strong
correlation between the reported contact with cat or raw consumption and the
personality profile suggests that the subjective factors play an important role
in questionnaire-based epidemiological studies. (It cannot be excluded, that
the cat owners or the raw meat eaters really have different personality
profiles than the general population.) It can be only recommended that in
epidemiological studies more objective questions like "When did you play
with a cat last time?" or "Did you eat a raw meat during past month
(past year)?" should be substituted for the subjective questions like
"Do you often play with a cat?" or "Do you often eat raw
meat?". Even then the results can be obscured by subjects who provide an
incorrect information during the interview. Publishing of questions and of
whole frequency tables in papers is necessary in order to make possible the
evaluation of impact of these effects. In our file of 30 questionnaire-based
epidemiological papers on toxoplasmosis only one provided the frequency tables
(31) and two presented the concrete questions given to the probandi (32,25).

It is known that personality
profiles of people with latent toxoplasmosis differ from those of noninfected
population (7,8). Our present results indicate that subjective interpretation
of reality influences a character of the person's answers in an interview. It
might be speculated that the correlation between the consumption of raw meat
and the toxoplasmosis may reflect only a fact that both the probability
reporting the consumption of raw meat and the probability of acquiring the
toxoplasmosis depend on the same factor, namely on the personality profile of
the subject. Our present results, namely the absence of correlation between the
reported consumption of raw meat and the personality factors influenced by
latent toxoplasmosis, however, suggest that this explanation is probably
incorrect. At the same time, the existence of highly significant correlation
between contact with cat and raw meat consumption could explain the reported
positive association between toxoplasmosis and the cat ownership.

Acknowledgments

We thank Dr. J. Kulda and Dr.
I. Hrdý for help with collecting the experimental data.This
research was supported by Grant Agency of Czech Republic grant 206/95/0638.